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1 Centre de recherche, Hôpital Laval, Institut universitaire de cardiologie et de pneumologie de l'Université Laval, Quebec City, Quebec, Canada 2 The First Affiliated Hospital of China Medical University, Shen Yang City, Liao Ning Province, China 3 Service de Pneumologie et réanimation, Groupe Hospitalier Pitié-Salpêtrière, Assistance Publique – Hôpitaux de Paris, Paris, France 4 UPRES EA 2397, Université Paris VI Pierre et Marie Curie, Paris, France
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Abstract |
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(Received 28 February 2007;
accepted after revision 29 March 2007; first published online 5 April 2007)
Corresponding author F. Sériès: Centre de Pneumologie Hôpital Laval, 2725, Chemin Sainte-Foy, Sainte-Foy, Quebec, Canada G1V 4G5. Email: frederic.series{at}med.ulaval.ca
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Introduction |
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Transcranial magnetic stimulation (TMS) can be used to explore certain aspects of the cortical control of skeletal muscle. Single-pulse TMS elicits motor-evoked potentials (MEP) that give information on the corticospinal pathway governing the studied muscle (Benecke et al. 1988; Claus, 1990; Di Lazzaro et al. 1999). From a functional point of view, for a given muscle, the corticospinal activation process can be characterized through the effects of stimulating conditions on the characteristics (amplitude and latency) of the MEPs. For example, the response to TMS is facilitated in the presence of an underlying voluntary contraction, with a shortening in the latency of MEPs and an increase in their amplitudes. The response of the Dia to TMS without facilitation and the effects of voluntary contractions have been described in normal individuals (Similowski et al. 1996a). In this muscle, there are facilitating effects of corticospinal inputs (voluntary contractions; Lissens, 1994; Davey et al. 1996; Similowski et al. 1996b) and of bulbospinal inputs (Murphy et al. 1990; Straus et al. 2004; Mehiri et al. 2006). Transcranial magnetic stimulation responses of tongue muscle, including the genioglossus (GG), which is one of the main UA dilators, have also been described (Meyer et al. 1997; Ghezzi & Baldini, 1998).
Many studies have established the importance of a precise coupling between the contractions of the UA dilator muscle and of inspiratory muscles. During automatic breathing, the inspiratory command originating from the brainstem respiratory central pattern generators is distributed first to UA dilator muscles and then to the Dia and to accessory inspiratory muscles. The beginning of the phasic activation of the UA dilators precedes that of inspiratory muscles; their peak activity is reached before that of the diaphragm (Strohl et al. 1980; Van Lunteren et al. 1983). This coupling is dynamic in nature, as demonstrated by the effects of CO2-induced hyperventilation and sleep on the pre-activation delay (Strohl et al. 1980). In humans, the alteration of this finely tuned synchronization has important clinical consequences because it is associated with the occurrence of UA closure during sleep (Hudgel & Harasick, 1990). Experimentally, the lack of preactivation of UA inspiratory muscles can be modelled through phrenic stimulation techniques to study the detrimental effect of such lack of preactivation on UA dynamics (Sériès et al. 1999).
The neuroanatomical coupling and the physiological basis of this coupling have been well described in various animal models (Kuna & Remmers, 1999; Peever et al. 2002; Shintani et al. 2003). However, despite the impact of the link between the activation process of the diaphragm and UA muscles on ventilatory output, there is no information in the literature on the interaction between Dia and GG corticomotor activities in humans and on the effects of facilitatory manoeuvres on corticomotor responsiveness.
We hypothesized that there is an interaction between the corticomotor activity of respiratory and UA muscles and that this interaction may be influenced by various manoeuvres aimed at preferentially facilitating one or the other pathway. Thus, the aim of the present study was to characterize the diaphragmatic and genioglossal corticospinal responses and their response to respiratory and non-respiratory manoeuvres using TMS in awake normal subjects.
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Methods |
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The study was conducted in Laval hospital research centre. Fifteen healthy volunteers (all males) participated in this study. A conventional full-night in-laboratory polysomnographic study (Sandman 4.1, Nellcor Puritan Bennett Ltd, Kanata, Canada) was completed in every subject to ascertain the absence of sleep-disordered breathing. No subject was taking medication or had any symptoms suggestive of respiratory disease, obstructive sleep apnoea or neurological disease. All had normal nighttime sleep behaviour. All experiments were conducted in accordance with the Declaration of Helsinki. Laval hospital internal review board approved this protocol and written informed consent was obtained from each subject.
Measurements
Electromyogram. Surface recording of the right and left costal diaphragmatic EMG activities was obtained by silver cup electrodes placed on the mid-clavicular line in the seventh to eighth right and left intercostal spaces. Genioglossus EMG activity was recorded by intraoral electrodes mounted on a mouthpiece made from a dental impression and lying on the anterior part of mouth floor as described by Doble et al. (1985). A surface EMG of dominant-sided abductor pollicis brevis (APB) was simultaneously recorded with silver cup electrodes. Electromyogram signals were sampled at 10 000 Hz, filtered (10 Hz to 1 kHz) and amplified (Grass CP122, Grass Instruments Co., West, Warwick, RI, USA). The GG EMG activity was rectified and integrated with a moving averager using a time constant of 50 ms (MA 1000, CWE, Ardmore, PA, USA). Swallowing, maximal protrusion of the tongue over the alveolar ridge and a Müeller manoeuvre were completed to determine the maximal GG voluntary activity.
Flow. A tight-fitting nasal continuous positive-pressure mask was placed over the nose with its airtightness being assessed by occlusion of its opening during maximal inspiratory efforts. Instantaneous flow was obtained from a pneumotachograph (Hans Rudolph, model 112467-3850A, Kansas City, MI, USA) connected to the mask. During part of the experiment, a unidirectional three-way valve was connected to the pneumotachograph and a 100 cmH2O l–1 s resistance was fixed on its inspiratory side. Subjects were studied lying in a comfortable armchair with a 60 deg inclination and with the head supported by a premolded firm pillow to make certain that head and neck were kept in the same position during the whole experiment.
Study design
No alcohol consumption was requested during the 2 days preceding the study. All measurements were made with subjects breathing exclusively through the nose. Transcranial magnetic stimulation was performed using a Magstim 200 stimulator (Magstim, Whitland, UK) with a 90 mm circular coil or a focal 70 mm figure-of-eight coil. For each stimulation site, the position of the coil was kept constant by attaching the coil handle to a high-precision multipositional support consisting of two articulated arms (MAN 143, Manfrotto Trading, Milano, Italy). Diaphragmatic response to TMS was assessed with the coil placed at the vertex or 1 cm posterior to the vertex to obtain the higher MEP amplitude (Murphy et al. 1990). In order to obtain the individual optimal GG response to TMS, the area anterolateral (AL) to the vertex of the dominant side, corresponding to the region 0–6 cm anterior and 6–10 cm lateral to the vertex, was divided into a 2 x 2 cm grid using an EEG skin china marker. The coil was successively centred on each intersection point to identify the best responsive site (Meyer et al. 1997). For convenience, this site was designed as the AL TMS site. The stimulator discharge was triggered by a timer driven by the changes in flow direction. The order in which Dia and GG TMS was applied was randomly determined. Subjects were not informed of the time when TMS was applied.
Considering the different neuromuscular activation profile of Dia and UA muscles during the breathing cycle (Van Lunteren et al. 1983), two different sets of experiments were conducted to evaluate the influence of respiratory timing and efforts on Dia and GG responses to TMS. During the first set (n = 10), TMS was applied in random order in four different conditions at each stimulation site: 0.5 s after the onset of quiet expiration (Exp 0.5 s); 0.5 s after the onset of quiet expiration with maximal pushing of the tongue against the maxillar ridge (Push); 1 s after the onset of quiet inspiration (Insp 1 s); and 1 s after the onset of inspiration with application of a fixed inspiratory resistance (Resist). During the second set of experiments (n = 6), TMS was applied at the end of quiet expiration (End Exp), 0.5 s after the onset of quiet inspiration (Insp 0.5 s) and at the end of a deep inspiration (D-Insp). Subjects were blind to the stimulation timing. In order to evaluate the effects of co-stimulation of GG and Dia corticomotor areas on measured variables, End Exp, Insp 0.5 s, D-Insp and Push manoeuvres were additionally completed with a focal coil positioned in AL TMS in eight subjects. The coil was placed to obtain an anticlockwise current. For each location and condition, five stimuli were delivered at 100% stimulator output intensity. During the 90 mm circular coil experiments, the intensity was then decreased stepwise to identify the Dia or GG respective motor thresholds that corresponded to the lowest stimulator output that elicited a 50 mV response on at least three out of five stimulations.
Data and statistical analysis
All EMG, flow and pressure tracings were recorded on a microcomputer (AxoScope software 9.0, Axon Instruments, Inc., Union City, CA, USA). For each muscle, EMG response was assessed by measuring MEP latency and amplitude. Response latency was defined as the time up to the first deflection from baseline following magnetic stimulation, and MEP amplitude was measured from peak to peak MEP response.
The multivariate normality was verified using the Mardia test. The univariate normality assumptions were verified with the Shapiro–Wilk test, and the Brown and Forsythe's variation of Levene's test statistics was used to verify the homogeneity of variances between stimulation site and among stimulation conditions.
We first assessed the difference in MEP characteristics between each muscle for each TMS site and stimulation condition. A multivariate repeated measures design was used, in which subjects were considered as random block effects, and MEP responses and individual stimuli were analysed as repeated measures. In order to evaluate the influence of stimulation conditions on MEP characteristics for each muscle and TMS site and the influence of TMS site on MEP characteristics for each muscle and stimulation condition, a split plot design was performed, considering subjects as random block effects and using individual stimuli as a repeated autoregressive structure.
Data are expressed as means ±
S.D or means ±S.E.M. The results were considered significant with P values 
0.05. The data were analysed using the statistical package program SAS version 9.1.3 (SAS Institute Inc., Cary, NC, USA).
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Results |
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Characteristics of EMG activity at the time of TMS application
Among the different studied conditions, GG EMG activity preceding TMS was significantly higher when pushing the tongue (53.3 ± 32.4% max) than in any other condition (End Exp in AL: 15.9 ± 6.8% max) in each TMS location. For a given condition, no difference was observed in the level of GG EMG activity between the vertex and AL (End Exp at the vertex: 13.2 ± 5.1% max).
Motor-evoked potential characteristics irrespective of TMS site and stimulation condition
Figure 1 represents typical examples of Dia, GG and APB EMG responses to proto-expiratory TMS. In most cases, vertex TMS and AL TMS evoked combined GG and Dia responses (Table 1). Isolated GG responses occasionally occurred but no diaphragmatic response was ever observed alone. Responses of APB were consistently recorded during both vertex and AL TMS. In all cases, the GG response came first, the Dia second and the APB last. The mean values of MEP latencies and amplitudes are represented in Tables 2 and 3, respectively.
Motor-evoked potential characteristics as a function of stimulation condition and TMS site
In the two sets of experiments and in almost all conditions, MEP GG latency was shorter when TMS was applied in AL than at the vertex (end-expiration values: 6.2 ± 3.4 and 9.7 ± 1.7 ms, respectively; Table 2) with no difference in Dia latencies between each stimulation site. Diaphragmatic MEP amplitudes did not differ between AL and vertex in any condition. In AL, the GG MEP amplitude was higher than that of Dia in any given condition (end-expiration values: 1.03 ± 0.24 and 0.86 ± 0.62 mV, respectively; Table 3).
First set of experiments (Exp 0.5 s, Insp 1 s, Push and Resist). The MEP characteristics of APB were not influenced by the conditions of TMS. In each TMS site, tongue pushing was associated with a significant decrease in GG MEP latency compared with other conditions. Diaphragmatic MEP latency was not influenced by respiratory conditions at the vertex but significantly decreased in AL during tongue protrusion and resistive inspiration (Table 2). Except for tongue protrusion, MEP GG amplitude was higher when TMS was applied in AL than at the vertex in the different conditions (Table 3). Genioglossus and Dia MEP amplitudes were not significantly influenced by respiratory conditions in AL. However, both responses significantly increased when TMS was applied at the vertex during tongue protrusion, with a remarkable rise in GG amplitude (0.5 s expiration and tongue protrusion: 0.59 ± 0.04 and 1.47 ± 0.03 mV, respectively; Table 3).
Second set of experiments (End Exp, Insp 0.5 s and D-Insp). For each TMS site, deep inspiration led to a significant decrease in GG and Dia latency compared with other conditions except for GG in AL (Table 2). Genioglossus MEP amplitudes were influenced by respiratory conditions, with a significant increase with deep inspiration, which was particularly marked at the vertex (0.5 s expiration and deep inspiration: 0.75 ± 0.18 and 1.29 ± 0.23 mV, respectively; Table 3). This effect of deep inspiration on Dia MEP amplitude was observed at both TMS sites (Table 3).
Assessment of Dia and GG overlap responses to TMS
In order to evaluate to what extent Dia responses during AL and vertex TMS could result from the overlap of the magnetic field over the two areas, in six subjects Dia MEP amplitude was measured at the nearest point from the vertex in the AL area in addition to measurements in vertex TMS and at the optimal AL site for GG response. Diaphragmatic MEP amplitude decreased from 1.17 ± 0.35 mV during AL to 0.56 ± 0.12 mV when moving towards the vertex (P = 0.007 with AL value), and increased again to 0.93 ± 0.34 mV at the vertex (P = 0.2 with AL). In one subject, Dia MEP response progressively vanished from AL to the vertex.
Focal TMS always induced a GG MEP response, whereas Dia responses were only seen in two subjects. Genioglossus latency and amplitude were significantly modified during facilitatory manoeuvres even in the absence of a Dia response, with a significant decrease in latency and increase in amplitude during deep inspiration and tongue protrusion (Table 4).
Transcranial magnetic stimulation motor thresholds
In any location and condition, the Dia motor threshold was higher than that of GG except for D-Insp at the vertex (P < 0.01; Table 5). Tongue protrusion and deep inspiration were associated with the lowest muscle threshold values, but the difference did not reach significance in the latter case. Genioglossus motor threshold was systematically lower when TMS was delivered at AL than at the vertex. Deep inspiration abolished this difference in motor threshold between GG and Dia when TMS was performed at the vertex.
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Discussion |
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Considering the lack of specificity of TMS applied with the circular coil, further illustrated by the presence of APB responses from both vertex and AL TMS, it is not surprising for us to find coupled Dia and GG responses. When the circular coil was used, it is most likely that vertex TMS performed to study the response of the Dia co-stimulated the GG corticomotor pathway because of the shape and size of the magnetic field. Similarly, AL TMS should co-stimulate GG and Dia, at least on the edge of the magnetic field. Owing to the disproportion in size of the Dia and GG respective cortical representation, this co-stimulation is expected to vanish with the decrease of AL TMS intensity. We observed this pattern in our subjects, where the Dia response decreased until the point of disappearance when TMS was brought down to low intensities whereas the GG response persisted. In contrast, the GG and Dia facilitatory manoeuvres did not influence the APB responses, indicating that changes in corticomotor excitability were limited to respiratory and UA muscles. Furthermore, with TMS applied focally in the GG cortical area, inspiratory manoeuvres had a facilitatory effect on GG corticomotor excitability even in the absence of Dia response. Therefore, reciprocal changes in the Dia and GG responses induced by facilitatory manoeuvres should truly reflect functional coupling, beyond the issue of co-stimulation.
The GG–Dia coupling was most apparent during facilitatory manoeuvres of respiratory nature. Voluntary deep inspiration significantly decreased MEP latency and increased MEP amplitude in both muscles for vertex TMS. The facilitatory effect of deep inspiration on Dia activity has been previously reported (Davey et al. 1996; Zifko et al. 1996) but its simultaneous effect on the activity of upper airway muscles had not yet been identified. Results obtained with focal TMS applied in AL demonstrated that, even in the absence of Dia response, deep inspiration has a facilitatory effect on GG activity. This further supports the strong functional link that exists between Dia and GG corticomotor excitatory pathways during respiratory manoeuvres. In contrast, the absence of facilitatory effect observed for GG between expiration and inspiration with or without resistance can be accounted for by an insufficient amount of phasic activity developed in these conditions. This might result from the specific neuromuscular activation profile of the upper airway muscles (rapid rise and plateauing in activity of UA muscles compared with a progressive rise in Dia activity throughout inspiration) and of the related differences in depolarization of phrenic and hypoglossal motoneurones. Caution should be taken before extrapolating the facilitatory effect of deep inspiration that we observed for GG to upper airway muscles in general. This effect relates to the summation of automatic/voluntary contraction and TMS-induced multiple neuronal discharges on the depolarization of spinal motoneurones (Day et al. 1987; Thompson et al. 1991; Lissens 1994). Hence, this phenomenon partly depends on the pre-activation of spinal motoneurones (Maertens de Noordhout et al. 1992; Cowan et al. 1986), which arises from muscle spindles and is carried out by Ia fibres. Considering the differences in proportion of muscle fibre types between the different upper airway muscles (Sériès et al. 1996), the effect of facilitatory manoeuvres could potentially differ among UA dilators.
In both GG and Dia muscles, no facilitatory effect was observed during tidal inspiration and resistive inspiration. This may contrast with the results of previous studies examining the facilitatory effect of tidal inspiration (Straus et al. 2004) and inspiratory resistance (Locher et al. 2006) on Dia corticomotor response. However, these studies differed from ours in their design, with an earlier timing at which TMS was applied during inspiration and with differences in the amount of inspiratory loading (Locher et al. 2006). Such differences can be accounted for by the preferential recruitment of non-diaphragmatic inspiratory muscles during inspiratory resistive loading (Jonville et al. 2005).
Conversely, during tongue protrusion, no evident Dia facilitation occurred. This absence of cross-facilitation between GG and Dia suggests that the activation of the GG corticospinal pathway can bypass the Dia corticospinal activity during non-respiratory tasks. Such functional independency is inherent to the numerous non-respiratory functions of UA muscles that are controlled by cortical activity (speech, eating, swallowing, etc.). This suggests that the occurrence of cross-facilitation during inspiratory manoeuvres depends on the activation of ‘respiratory programs’. This raises the issue of putative corticobulbospinal respiratory pathways. Indeed distinct fast-conducting pathways have been described that connect the cerebral cortex to the brainstem lingual motor nuclei in humans (Meyer et al. 1997; Ghezzi & Baldini, 1998) and to the human diaphragm (Gandevia & Rothwell, 1987; Similowski et al. 1996b;). Such corticospinal pathways are known to originate from different cortical areas, as illustrated by pioneering studies conducted by Foerster on the mapping of the human motor cortex (Foerster, 1936). The AL area has been shown to be the optimal site for the investigation of GG response to TMS (Meyer et al. 1997; Rodel et al. 2003). In contrast, even if the cortical excitation of Dia motoneurones is usually considered to transit via a direct corticospinal pathway (Urban et al. 2002), corticobulbar pathways may exist (Murphy et al. 1990; Chang, 1992) that could be called upon to explain some of our observations.
The neuromuscular activity of UA muscles and Dia are similarly affected by changes in the central respiratory drive, as assessed by the parallel enhancement in their activities induced by hypoxia, hypercapnia and increased inspiratory resistance (Onal et al. 1981; Patrick et al. 1982). In any case, activity of UA muscles preceeds that of the diaphragm (Strohl et al. 1980; Van Lunteren et al. 1983). This pre-activation pattern of the UA muscles requires that, in addition to the input of the hypoglossus nucleus, the hypogossal motoneurone activity is modulated by other inputs originating from respiratory neurone groups. This is supported by animal studies showing that the Kölliker–Fuse nucleus, which belongs to the pneumotaxic centre, containing respiratory neurones, produces a selective premotor input to hypoglossal motoneurones (Kuna & Remmers, 1999). Furthermore, individual medullary reticular formation neurones could provide inputs to both genioglossal and diaphragmatic motoneurones (Shintani et al. 2003), and some neurones in the lateral tegmental area contribute to the respiratory control of hypoglossal motoneurones and Dia (Peever et al. 2002). Such interaction between Dia and GG motoneurone activities is further supported by the inhibitory effect of serotonin antagonists on inspiratory phasic activity of both the phrenic and hypoglossal motoneurone pools (Rose et al. 1995; Richmonds & Hudgel, 1996).
In our study, the motor threshold of GG was consistently lower than that of Dia. This could be explained by the difference in size of the respective GG and Dia motor cortex representation (Foerster, 1936). However, given the fact that the influence of TMS site on motor threshold was not observed for the Dia (except for resistive inspiration), these observations are also compatible with a lower TMS response threshold/enhanced excitability at the GG cortical area.
Considering the dramatic influence of sleep on the neuromuscular activation pattern (Grosse et al. 2002; De Gennaro et al. 2004) and its role in the occurrence of obstructive breathing disorders (Day et al. 1987; Horner 1996), as well as the influence of sleep on the inspiratory-related Dia facilitation (Mehiri et al. 2006), further studies are required to document the influence of sleep on the corticomotor responsiveness of both Dia and UA muscles and to explore its potential implication in the occurrence of sleep-induced breathing disorders.
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